Phytoparasitica https://doi.org/10.1007/s12600-019-00781-8

Biodiversity of the natural enemies of (: ) in Northwest Turkey

Şahin Kök & Željko Tomanović & Zorica Nedeljković & Derya Şenal & İsmail Kasap

Received: 25 April 2019 /Accepted: 19 December 2019 # Springer Nature B.V. 2020

Abstract In the present study, the natural enemies of (), as well as eight other generalist natural aphids (Hemiptera: Aphididae) and their host in- enemies. In these interactions, a total of 37 -natural cluding herbaceous plants, shrubs and trees were enemy associations–including 19 associations of analysed to reveal their biodiversity and disclose Acyrthosiphon pisum (Harris) with natural enemies, 16 tritrophic associations in different habitats of the South associations of trifolii (Monell) with natural Marmara region of northwest Turkey. As a result of field enemies and two associations of Aphis craccivora Koch surveys, 58 natural enemy associated with 43 with natural enemies–were detected on Medicago sativa aphids on 58 different host plants were identified in the L. during the sampling period. Similarly, 12 associations region between March of 2017 and November of 2018. of cerasi (Fabricius) with natural enemies were In 173 tritrophic natural enemy-aphid-host interac- revealed on avium (L.), along with five associa- tions including association records new for Europe and tions of brassicae (Linnaeus) with natural Turkey, there were 21 representatives of the enemies (including mostly individuals) on (Coleoptera), 14 of the family Syrphidae oleracea L. Also in the study, reduviids of the (Diptera) and 15 of the subfamily species renardii (Kolenati) are reported for the first time as new potential aphid biocontrol agents in Turkey. The results of field surveys show that the natural enemies Ş. Kök (*) : İ.Kasap of aphids have high biodiversity, which should be con- Department of Plant Protection, Faculty of Agriculture, Çanakkale sidered in the management of . Onsekiz Mart University, TR-17020 Çanakkale, Turkey e-mail: [email protected] Keywords Biological control . Aphididae . e-mail: [email protected] Coccinellidae . . Aphidiinae . South Marmara Ž. Tomanović Faculty of Biology, Institute of Zoology, University of Belgrade, Studenstki trg 16, Belgrade 11000, Serbia Introduction Z. Nedeljković BioSense Institute-Research Institute for Information Technologies in Biosystems, Dr Zorana Đinđića1,Novi As one of the most important of agricultural pests, Sad 21000, Serbia aphids (Hemiptera, Aphididae) cause severe significant economic losses and are distributed in most terrestrial D. Şenal Department of Plant Protection, Faculty of Agriculture and Natural ecosystems throughout the world. They damage agri- Sciences, Bilecik Şeyh Edebali University, cultural crops, forest plants and shade trees, especially in TR-11230 Bilecik, Turkey temperate regions, as a result of sap-sucking, Phytoparasitica secretion and transmission of phytopathogenic viruses habitats of the South Marmara region of northwest (Alford 2011; Diehl et al. 2013). Turkey, which is an important crossroad between Eu- Natural enemies, including specialist and generalist rope and Asia and has a rich and diverse flora and fauna. species, play a very important role in suppressing pop- ulations of aphids and other herbivores (Symondson et al. 2002;Luetal.2012), Such natural Material and methods enemies affect at least 50% of all aphid species on the surface of the earth (Waage 1991). Up to now, about Sampling area 2000 , generally consisting of parasitoid spe- cies, have been determined as biological control agents Our sampling area, the South Marmara region in north- worldwide (van Lenteren et al. 2006). Aphids are usu- west Turkey, consists of the Çanakkale and Balıkesir ally attacked by natural enemies such as , Provinces, which constitute an important link between predators and some pathogens. Of these, both the larvae Europe and Asia. This area includes 3% of Turkey’s and the adult stages of coccinellid species are preda- land, with a surface area of 783.562 km2, and it is an ceous on aphids, while only the larval stages of syrphids outstanding region in terms of agricultural production. and chrysopids are predaceous on them. Also among The region has a continental climate in the southeastern parasitoids, species belonging to the family Braconidae parts, milder climate in parts close to the coastal area and (especially members of the subfamily Aphidiinae) de- Mediterranean climate in regions of the gulf and islands. velop as solitary endoparasitoids on aphid populations The sampling area also includes wilderness areas such (Völkl et al. 2007). as the Edremit Gulf, Biga Peninsula, Gallipoli Peninsula Surveying the biodiversity of natural enemies of and Kaz Dağları (Ida Mountains), which are known to herbivore pests in both agricultural and natural habitats have a high degree of endemic floristic and faunistic is quite important from the standpoint of planning bio- diversity (Özhatay and Özhatay 2005). logical control strategies. A richness of natural enemies makes possible stronger biological control in all habitats Collection and identification of aphids and their natural (Letourneau et al. 2009; Griffin et al. 2013; Katano et al. enemies 2015). When the taxonomic distance between natural enemies on herbivore pests was high, the effect of this Specimens of aphids and their natural enemies were phenomenon was likewise positive (Griffin et al. 2013). collected from their host plants, including herbaceous However, greater diversity of natural enemies can lead plants, shrubs and trees in different habitats such as to more ineffective pest control in agricultural habitats cultivated (simple landscapes-1), uncultivated (Snyder and Wise 2001; Montoya et al. 2003). (complex landscapes-2) and urban areas (3) in the In addition, the nature of associations of aphid and Çanakkale and Balıkesir Provinces in northwest Turkey their host plants in different habitats can regulate the between March of 2017 and November of 2018. Ac- efficacy of influence exerted by specialist and generalist cordingly, all samples were marked in the catalogue of natural enemies on aphid populations. According to the associations. Sufficient numbers of apterous and alate hypothesis of host physiological phenotype, host plants specimens of aphids were transferred with a soft brush that are nutrient-rich and short-lived tend to increase the to Eppendorf tubes containing 70% ethyl alcohol for density of aphids (Cronin et al. 2010), as in the case of identification. The aphid specimens were identified by populations of other nitrogen-limited herbivores the first author using a LEICA DM 2500 microscope (Mattson 1980), because host plants with a great amount with a mounted HD camera and LAS software (version of nitrogen have a positive effect on the development of 4.1) according to Blackman and Eastop (2006, 2018) aphid populations (Schütz et al. 2008). In view of the and Kök et al. (2016); Kök and Kasap (2019). Adults of aforementioned considerations, the biodiversity of nat- natural enemies, especially ladybirds, and ural enemies and their interactions with both pests and generalist predators such as representatives of host plants were here investigated in detail so as to better Hemiptera, Dermaptera and , were collected understand enemy-herbivore-host plant associations. from host plants infested with aphids by visual and hand The aim of the present study was to reveal biodiver- searching using sweep nets and suction tubes, after sity of the natural enemies of pest aphids in different which they were brought to the laboratory in plastic Phytoparasitica boxes and glass jars for preparation and identification. hoverflies, are one of the most common known natural For sampling of predator larvae and parasitoids, differ- enemies of aphid populations (Chambers 1988) and are ent parts of aphid-infested plants including predator important agents for the biological control of many pests larvae and mummified aphids were brought in the same under both agricultural and greenhouse conditions boxes to the laboratory for emergence of adult speci- (Pineda and García 2008; Leroy et al. 2010; Amorós- mens. The larvae of predators were kept until they were Jiménez et al. 2012). The most effective of them, larvae adults in the aphid-containing plastic boxes, the upper of the species Episyrphus balteatus de Geer, feed on part of which was covered with a net. For parasitoid about 100 aphid species throughout the world (Sadeghi emergence, mummified individuals in aphid colonies on and Gilbert 2000). In the same vein, Bayrak and Hayat the host plants were put in plastic bottles and kept in (2008)statedthatE. balteatus preys on 33 aphid species laboratory conditions (22.5 °C, 65% humidity, 16:8 L:D and is common in many regions of Turkey. Similarly, photoperiod). After the emergence of adult predators we found that the larvae of this species feed on and parasitoids, the specimens of natural enemies of 10 aphid species harmful to many cultivated plants and aphids were sent to competent experts for identification. are commonly encountered in our study area. Specimens belonging to the subfamily Aphidiinae Among the most notable details in the catalogue of (Braconidae) and families Syrphidae and Coccinellidae tritrophic relationships given below are the aphid- were identified by the second, third and fourth authors, natural enemy associations on Medicago sativa L. Al- respectively. Permanent slides of identified aphids and falfa (M. sativa) is the most widely used fodder crop ladybird specimens were deposited in the library of worldwide (Walton 1983) and some aphid species such slides maintained by the Department of Plant Protection, as Acyrthosiphon pisum (Harris); Acyrthosiphon kondoi Faculty of Agriculture, Çanakkale Onsekiz Mart Uni- Shinji; Therioaphis trifolii and Aphis craccivora have versity. Specimens of other natural enemies were depos- been reported as major pests of fields in different ited in personal collections of the identifying experts. parts of the world (Summers 1976; Nakashima and Akashi 2005; Rakhshani et al. 2006). These fields can also serve as rich reservoir areas for the natural enemies Results and discussion of aphids (Summers 1998) and researching the associa- tions between aphids and their natural enemies in alfalfa In determining biodiversity of the natural enemies of fields is important to improve biological control strate- aphids in the present study, 58 natural enemy species gies. As a result of sampling from different alfalfa fields, associated with 43 aphids on 58 different host plants we detected a total of 37 associations of aphids with were recorded in different habitats of the South natural enemies, including 19 associations of A. pisum Marmara region of northwest Turkey during surveys with natural enemies, 16 associations of T. trifolii with conducted from 2017 to 2018. These enemies included natural enemies and two associations of A. craccivora 21 species of ladybird of the family with natural enemies on M. sativa during the sampling Coccinellidae (Coleoptera), whose members are one of period, as indicated in the catalogue below. Similarly, 12 the most frequently encountered natural enemies in all associations of M. cerasi with natural enemies on Pru- regions of Turkey. To be specific, Aslan and Uygun nus avium (L.) were revealed in this study, along with (2005) reported 33 coccinellid species feeding on 59 five associations of B. brassicae with natural enemies aphids in Kahramanmaraş and emphasized that the most (including mostly parasitoid individuals) on Brassica common enemy is Coccinella septempunctata Linnae- oleracea L. us, which was found feeding on 41 aphid species. Also, The surprising finding of (Kolenati), a Kök et al. (2017) determined that C. septempunctata is generalist predator of leafhoppers, is one of the most the most collected predator, with a 35,1% availability interesting results of the present study. This generalist is rate for aphids in Çanakkale, including our current sur- a species native to North and Central America, from vey area. These results are corroborated by the data we which it then began to spread to Hawaii and other obtained in the present study, in which associations tropical areas of the Pacific region (Weirauch et al. between C. septempunctata and 12 aphids were found 2012). The predator later reached Greece and the Balkan in the South Marmara region. Species of the family Peninsula, which are close neighbours of Turkey Syrphidae, widely recognized as aphidophagous (Davranoglou 2011; Simov et al. 2017). The first Phytoparasitica finding of Z. renardii in the Turkish fauna was recorded primary natural enemies of B. brassicae and Aphis by Çerçi and Koçak (2016)fromİstanbul and İzmir, glycines (Read et al. 1970; Zhu and Park 2005). Also, close to the European continent and the Balkan Penin- chemical and physical cues such as the alarm phero- sula. In another study, Z. renardii was determined as a mone honeydew, its smell, aphid body colour and the natural enemy of Glycaspis brimblecombei (Moore) shape and movement of aphids are effective factors feeding on Eucalyptus camaldulensis Dehnh (Yurt and enabling suitable prey aphids to be reached by both their Karaca 2018). Finally, Z. renardii associated with parasitoids and their predators (Michaud and Mackauer Cinara tujafilina (Del Guarcio) feeding on Platycladus 1994;Harmonetal.1998). In light of the foregoing orientalis is here determined for the first time as a considerations, we have catalogued below the natural predator of aphids in Turkey (in the South Marmara enemy-prey aphid-host plant associations in the South region). We feel that as a natural enemy, this generalist Marmara region of northwest Turkey so that these in- predator has the potential to be an agent for the biolog- teractions in different habitats can be better understood ical control of aphids, and that records of its finding will and used more effectively in strategies for the biological be reported from different habitats and regions of Tur- control of aphids. In the present study, 173 tritrophic key in years to come. However, it should not be forgot- natural enemy-aphid-host plant associations (including ten that Z. renardii is an intraguild predator of the larvae association records new for Europe and Turkey) were of (Stephens), an important agent determined that consisted of 58 natural enemies, 43 for the biological control agent of aphids (Rosenheim aphids and 58 different host plant species, as shownin et al. 1993; Cisneros and Rosenheim 1997). the catolague below. On the other hand, parasitoid species, generally taxa Catalogue of plant-aphid-predator/parasitoid associ- belonging to the subfamily Aphidiinae (Hymenoptera: ations from the South Marmara region of northwest Braconidae), are specialist natural enemies of aphid pop- Turkey. ulations and attack by laying their eggs in the body of nymphs and adult instars of their prey aphids (Bai and Amaranthus albus L. () Mackauer 1990; Ralec 1995). Up to now, a number of authors have conducted various studies to determine the Aphis craccivora Koch, 1854: *COCCINELLIDAE species of aphid parasitoids in many regions of Turkey, (Coleoptera): Hippodamia variegata Goeze, 1777 (1). and they have contributed new records for the Turkish *SYRPHIDAE (Diptera): tibialis (Fallén, fauna(ÖlmezandUlusoy2003; Aslan et al. 2004; Çetin 1817) (1). *Note: The association between ğ ć Erdo an et al. 2008; Tomanovi et al. 2008; Kök et al. A. craccivora and P. ti bi al is is recorded for the first time 2017). In the present study, we identified 15 parasitoid on host plants such as A. albus. species from the subfamily Aphidiinae (Hymenoptera: Braconidae) associated with 26 aphids feeding on 30 host Amaranthus retroflexus L. (Amaranthaceae) plant species. Also in this study, we collected as aphid natural enemies one species belonging to Chamaemyiida Aphis craccivora: *SYRPHIDAE (Diptera): P. tibialis (Diptera) and two species of hyperparasitoids that cannot (1). *Note: The association between A. craccivora and be identified. However, they were not included in the P.tibialis is recorded for the first timeon host plants such evaulation of tritrophic associations. as A. retroflexus. The interactions between aphids and their host plants are an important phenomenon affected by the nature of the habitat of host plants and aphids, location of the Apiaceae (unidentified plant species) habitat and acceptance of aphids as prey by their natural enemies. The odours emitted by aphid-uninfested plants Unidentified aphid species 1: *SYRPHIDAE (Diptera): are a powerful guide enabling natural enemies to easily Episyrphus balteatus (de Geer, 1776) (1). find their prey aphid on host plants in different habitats (Hatano et al. 2008). For example, (unidentified plant species) and methyl salicylate emitted by the host plants Brassi- ca oleraceae and Glycine max attract , Unidentified aphid species 2: *SYRPHIDAE (Diptera): C. septempunctata and syrphid , which are the Eupeodes corollae (Fabricius, 1794) (3); Eupeodes Phytoparasitica luniger (Meigen, 1822) (2); Meliscaeva auricollis Chenopodium album L. (Amaranthaceae) (Meigen, 1822) (3); pyrastri (Linnaeus, 1758) (3). Uroleucon sp.: *BRACONIDAE (Hymenoptera): Aphis fabae Scopoli, 1763: *BRACONIDAE (Hyme- Aphidius funebris Mackauer, 1961 (2); Praon yomenae noptera): Binodoxys angelicae (Haliday, 1833) (1). Takada,1968(2). Aphis solanella Theobald, 1914: *COCCINELLIDAE (Coleoptera): H. variegata (2). Hayhurstia atriplicis (Linnaeus, 1761): Berberis sp. (Berberidaceae) *SYRPHIDAE (Diptera): E. balteatus (1). *BRACONIDAE (Hymenoptera): B. angelicae (2); Liosomaphis berberidis (Kaltenbach, 1843): D. rapae (2). *COCCINELLIDAE (Coleoptera): Coccinella septempunctata Linnaeus, 1758 (3). Chrysanthemum sp. (Asteraceae) Berberis thunbergii DC. (Berberidaceae) Glover, 1877: *BRACONIDAE (Hyme- L. berberidis: *COCCINELLIDAE (Coleoptera): noptera): Aphidius colemani Viereck, 1912 (3). C. septempunctata (3); Harmonia axyridis Pallas, 1773 (3); H. variegata (3). Crepis sp. (Asteraceae)

Brassica oleracea L. () A. gossypii: *BRACONIDAE (Hymenoptera): Aphidius matricariae Haliday, 1834 (2). Brevicoryne brassicae (Linnaeus, 1758): *COCCINELLIDAE (Coleoptera): C. septempunctata (1). *SYRPHIDAE (Diptera): E. corollae (1); Cupressus arizonica Greene (Cupressaceae) S. pyrastri (1); (Meigen, 1822) (1). *Note: The association between S. selenitica and Cinara fresai Blanchard, 1939: *COCCINELLIDAE B. brassicae is recorded for the first time in Turkey. This (Coleoptera): Adalia decempunctata (Linnaeus, 1758) relationship was previously documented only from Po- (3); C. septempunctata (3); Nephus includens (Kirsch, land (Malinowska 1973;Rojoetal.2003). 1870) (3). *BRACONIDAE (Hymenoptera): Diaeretiella rapae (Curtis, 1860) (1). Cydonia oblonga mill. ()

Capsella rubella Reut. (Brassicaceae) Ovatus insitus (Walker, 1849): *COCCINELLIDAE (Coleoptera): A. bipunctata (1); C. septempunctata (1). Aphis craccivora: *BRACONIDAE (Hymenoptera): Lysiphlebus fabarum (Marshall, 1896) (2); (Cresson, 1880) (2). Cynara scolymus L. (Asteraceae)

Carlina sp. (Asteraceae) cardui (Linnaeus, 1758): *SYRPHIDAE (Diptera): E. balteatus (1). Uroleucon jaceae (Linnaeus, 1758): *BRACONIDAE (Hymenoptera): P. yomenae (2). Cynara sp. (Asteraceae)

Catalpa bignonioides Walter (Bignoniaceae) B. cardui: *COCCINELLIDAE (Coleoptera): C. septempunctata (2). *SYRPHIDAE (Diptera): Aphis Mamontova, 1953: *COCCINELLIDAE S. selenitica (2). *Note: This is a new aphid-syrphid (Coleoptera): (Linnaeus, 1758) (3). association according to Rojo et al. 2003. Phytoparasitica

Cynoglossum creticum mill. () Malus floribunda Siebold ex Van Houtte (Rosaceae)

Acyrthosiphon malvae (Mosley, 1841): Aphis pomi De Geer, 1773: *BRACONIDAE (Hyme- *COCCINELLIDAE (Coleoptera): C. septempunctata noptera): Lipolexis gracilis Forster, 1862 (3); (1); Scymnus pallipediformis Gunther, 1958 (1). Lysiphlebus cardui (Marshall, 1896) (3); L. fabarum (3).

Euphorbia rigida M.Bieb. (Euphorbiaceae) sp. ()

Aphis vallei Hille Ris Lambers & Stroyan, 1959: Aphis umbrella (Börner, 1950): *BRACONIDAE (Hy- *COCCINELLIDAE (Coleoptera): Scymnus apetzi menoptera): A. matricariae (2). Mulsant, 1846 (2). *SYRPHIDAE (Diptera): Scaeva albomaculata (Macquart, 1842) (2). *Note: This is a Malva sylvestris L. (Malvaceae) new aphid-syrphid association. Additionally, this syrphid species is found for the first time on a host plant A. umbrella: *BRACONIDAE (Hymenoptera): from the Euphorbia (Rojo et al. 2003). Lysiphlebus confusus Tremblay & Eady, 1978 (1). *BRACONIDAE (Hymenoptera): Ephedrus persicae Froggatt, 1904 (2). Matricaria sp. (Asteraceae)

Hedera helix L. (Araliaceae) Unidentified aphid species 2: *BRACONIDAE (Hyme- noptera): L. testaceipes (2). Aphis hederae Kaltenbach, 1843: *BRACONIDAE (Hymenoptera): B. angelicae (3). Medicago sativa L. (Leguminosae)

Acyrthosiphon pisum (Harris, 1776): syriacus L. (Malvaceae) *COCCINELLIDAE (Coleoptera) (1): A. decempunctata; C. septempunctata; Coccinula A. gossypii: *BRACONIDAE (Hymenoptera): quatuordecimpustulata (Linnaeus, 1758); Exochomus L. testaceipes (3). nigromaculatus Goeze, 1777; Hippodamia tredecimpunctata Linnaeus, 1758; H. variegata; Propylea Juniperus oxycedrus L. (Cupressaceae) quatuordecimpunctata (Linnaeus, 1758); Psyllobora vigintiduopunctata (Linnaeus, 1758); S. apetzi; Cynara oxycedri Binazzi, 1996: *BRACONIDAE (Hy- S. pallipediformis; Scymnus quadriguttatus Fürsch et menoptera): Pauesia sp. Quilis, 1931 (3). Kreissl, 1967. *SYRPHIDAE (Diptera) (1): E. balteatus; E. corollae; Melanostoma mellinum (Linnaeus, 1758); Lactuca sp. (Asteraceae) S. pyrastri; Sphaerophoria scripta (Linnaeus, 1758). *CHRYSOPIDAE (Neuroptera) (1): C. carnea. Acyrthosiphon lactucae (Passerini, 1860): *BRACONIDAE (Hymenoptera) (1): Aphidius ervi *BRACONIDAE (Hymenoptera): A. matricariae (2). Haliday, 1834; Aphidius banksae Kittel, 2016. Aphis craccivora: *COCCINELLIDAE (Coleoptera): Malus domestica Borkh. (Rosaceae) S. apetzi (1). *SYRPHIDAE (Diptera): S. pyrastri (1). Therioaphis trifolii (Monell, 1882): Dysaphis plantaginea (Passerini, 1860): *COCCINELLIDAE (Coleoptera) (1): A. bipunctata; *COCCINELLIDAE (Coleoptera): A. bipunctata (1); C. quatuordecimpustulata; E. nigromaculatus; N. includens (1). *CHRYSOPIDAE (Neuroptera): H. variegata; P. quatuordecimpunctata; Chrysoperla carnea (Stephens, 1836) (1). P. vigintiduopunctata; S. apetzi; S. pallipediformis; *BRACONIDAE (Hymenoptera): A. matricariae (1); Scymnus rubromaculatus (Goeze, 1778). *SYRPHIDAE E. persicae (1). (Diptera) (1): E. corollae; S. scripta; Sphaerophoria A. gossypii: *BRACONIDAE (Hymenoptera): rueppellii Wiedemann, 1830. *Note: The association B. angelicae (1); L. testaceipes (1). between S. rueppellii and T. trifolii is the first record in Phytoparasitica

Turkey. Before the present study, this association was P. tibialis is recorded for the first time on host plants confirmed only in Poland in Europe (Rojo et al. 2003). such as P. oleracea. *BRACONIDAE (Hymenoptera): Also, the E. corollae-T. trifolii and S. scripta-T. trifolii L. testaceipes (1). associations are recorded for the first time in Turkey, having been previosly known only from Poland in the Prunus avium (L.) L. (Rosaceae) whole Europe (Bankowska et al. 1975;Rojoetal.2003). *MIRIDAE (Hemiptera) (1): Deraeocoris serenus Myzus cerasi (Fabricius, 1775): *COCCINELLIDAE (Douglas & Scott, 1868). *NABIDAE (Hemiptera): (Coleoptera) (1): A. bipunctata; Adalia fasciatopunctata Nabis pseudoferus Remane, 1949. *CHRYSOPIDAE revelieri Mulsant, 1866; A. decempunctata; Chilocorus (Neuroptera) (1): C. carnea. *HEMEROBIIDAE bipustulatus (Linnaeus, 1758); H. axyridis; (Neuroptera) (1). O. conglobata. *SYRPHIDAE (Diptera) (1): E. balteatus; Paragus pecchiolii Rondani, 1857. *Note: Nerium oleander L. (Apocynaceae) The association of M. cerasi and E. balteatus is recorded for the first time in Turkey. Also, the association be- Aphis nerii Boyer de Fonscolombe, 1841: tween M. cerasi and P. pecchiolii is recorded for the first *COCCINELLIDAE (Coleoptera): A. bipunctata (3); time in Europe. *FORFICULIDAE (Dermaptera) (1): A. decempunctata (3); P. quatuordecimpunctata (3). Forficula aetolica Brunner, 1882; Forficula auricularia *BRACONIDAE (Hymenoptera): A. colemani (3); Linnaeus, 1758; F. smyrnensis. *BRACONIDAE (Hy- B. angelicae (3); L. testaceipes (3). menoptera): A. matricariae (1). Patch, 1914: *COCCINELLIDAE (Coleoptera): A. decempunctata (3); Prunus domestica L. (Rosaceae) P. quatuordecimpunctata (3). (Kaltenbach, 1843): Philadelphus coronarius L. (Hydrangeaceae) *COCCINELLIDAE (Coleoptera): P. quatuordecimpunctata (1). *SYRPHIDAE (Diptera): Aphis fabae mordvilkoi Börner & Janich, 1922: E. balteatus (1). *BRACONIDAE (Hymenoptera): *BRACONIDAE (Hymenoptera): L. testaceipes (3). E. persicae (1). Hyalopterus pruni (Geoffroy, 1762): Pistacia terebinthus L. (Anacardiaceae) *COCCINELLIDAE (Coleoptera): A. bipunctata (1). *SYRPHIDAE (Diptera): E. balteatus (1). Baizongia pistaciae (Linnaeus, 1767): * FORFICULIDAE (Dermaptera): Forficula smyrnensis Audinet-Serville, 1839 (1). Prunus dulcis (mill.) D.a.Webb (Rosaceae)

Hyalopterus amygdali (Blanchard, 1840): Platycladus orientalis (L.) Franco (Cupressaceae) *COCCINELLIDAE (Coleoptera): A. bipunctata (3). Cinara tujafilina (Del Guercio, 1909): *COCCINELLIDAE (Coleoptera): A. decempunctata Prunus persica (L.) Batsch (Rosaceae) (3); C. septempunctata (3); H. axyridis (3); Harmonia quadripunctata (Pontoppidan, 1763) (3); Oenopia Brachycaudus amygdalinus (Schouteden, 1905): conglobata (Linnaeus, 1758) (3); S. pallipediformis *COCCINELLIDAE (Coleoptera): C. septempunctata (3); Scymnus subvillosus (Goeze, 1777) (3). (1). * (Hemiptera): Zelus renardii (Kolenati, 1856) (3). Punica granatum L. (Lythraceae)

Portulaca oleracea L. (Portulacaceae) Aphis punicae Passerini, 1863: *COCCINELLIDAE (Coleoptera): A. f. revelieri (1). *BRACONIDAE (Hy- Aphis craccivora: *SYRPHIDAE (Diptera): P. tibialis menoptera): A. matricariae (1); B. angelicae (1); (1). *Note: The association between A. craccivora and L. testaceipes (1). Phytoparasitica

Pyracantha coccinea M.Roem. (Rosaceae) Solanum americanum Mill. ()

A. spiraecola: *COCCINELLIDAE (Coleoptera): A. solanella: *SYRPHIDAE (Diptera): S. pyrastri (1). A. bipunctata (3); H. axyridis (3). *SYRPHIDAE (Dip- tera): E. balteatus (3). *Note: This is an aphid-syrphid Sonchus sp. (Asteraceae) association new in Turkey. Hyperomyzus lactucae (Linnaeus, 1758): Rosa sp. (Rosaceae) *SYRPHIDAE (Diptera): E. balteatus (1); Paragus quadrifasciatus Meigen, 1822 (1). *Note: The associa- Macrosiphum euphorbiae (Thomas, 1878): tion between H. lactucae and P. quadrifasciatus is re- *COCCINELLIDAE (Coleoptera): C. septempunctata (2). corded for the first time in Turkey. This association was Macrosiphum rosae (Linnaeus, 1758): previously documented only in Spain (Marcos García *COCCINELLIDAE (Coleoptera): C. septempunctata 1981, 1985;Rojoetal.2003) and Portugal (Rojo et al. (3). *SYRPHIDAE (Diptera): E. balteatus (2); S. 2003). pyrastri (3). *Note: The association of M. rosae and E. balteatus is recorded for the first time in Turkey. vanhouttei (Briot) Zabel (Rosaceae)

Rumex crispus L. (Polygonaceae) A. spiraecola: *COCCINELLIDAE (Coleoptera): A. bipunctata (3). *SYRPHIDAE (Diptera): Aphis rumicis Linnaeus, 1758: *COCCINELLIDAE E. balteatus (3). *Note: This is an aphid-syrphid asso- (Coleoptera): Platynaspis luteorubra (Goeze, 1777) (2). ciation new in Turkey.

Rumex pulcher L. (Polygonaceae) Tamarix sp. (Tamaricaceae)

A. rumicis: *BRACONIDAE (Hymenoptera): Brachyunguis tamaricis (Lichtenstein, 1886): B. angelicae (1); L. fabarum (1). *COCCINELLIDAE (Coleoptera): A. decempunctata (3); H. variegata (3); O. conglobata (3).

Rumex sp. (Polygonaceae) Tribulus terrestris L. (Zygophyllaceae) A. solanella: *BRACONIDAE (Hymenoptera): B. angelicae (2); L. fabarum (2). Aphis craccivora: *SYRPHIDAE (Diptera): Paragus haemorrhous Meigen, 1822 (2). *Note: This is an aphid-syrphid relationship new in Turkey. The associa- Sambucus nigra L. (Adoxaceae) tion was previously recorded only in Spain (Rojo and Marcos García 1998;Rojoetal.2003) and Portugal Aphis sambuci Linnaeus, 1578: *COCCINELLIDAE (Gomes 1981;Rojoetal.2003). (Coleoptera): A. bipunctata (3); O. conglobata (3). Triticum aestivum L. (Poaceae) Scabiosa sp. (Caprifoliaceae) Sitobion avenae (Fabricius, 1775): *COCCINELLIDAE M. rosae: *COCCINELLIDAE (Coleoptera): (Coleoptera): C. quatuordecimpustulata (1). S. apetzi (2). Urtica urens L. (Urticaceae) Silybum marianum (L.) Gaertn. (Asteraceae) A. solanella: *SYRPHIDAE (Diptera): S. selenitica (2). A. fabae: *BRACONIDAE (Hymenoptera): *Note: This is a new aphid-syrphid association accord- L. testaceipes (2). ing to Rojo et al. 2003. Phytoparasitica

Veronica sp. (Plantaginaceae) Acknowledgements This manuscript is a part of the PhD thesis of the first author. The authors are grateful to Associate Professor Dr. Sinan Anlaş and Dr. Gülten Yazıcı for identifying the generalist A. gossypii: *COCCINELLIDAE (Coleoptera): predator specimens; Associate Professor Dr. Ersin Karabacak for C. septempunctata (2). *BRACONIDAE (Hymenop- identifying the host plant species; and Mr. Raymond Dooley for tera): B. angelicae (2). proofreading the revised version of the manuscript and editing the English. Zorica Nedeljković’s position at the University of Novi Sad is funded by the Ministry of Education, Science and Techno- Viburnum opulus L. (Adoxaceae) logical Development of the Republic of Serbia (project OI173002) and the H2020 project “ANTARES” (664387). The contribution A. spiraecola: *BRACONIDAE (Hymenoptera): of Željko Tomanović was supported by grant III43001 funded by L. fabarum (3); L. testaceipes (3). the Ministry of Education, Science and Technological Develop- ment of the Republic of Serbia.

Viburnum tinus L. (Adoxaceae) Compliance with ethical standards The authors declare that the work is in compliance with ethical standards. A. spiraecola: *COCCINELLIDAE (Coleoptera): A. bipunctata (3). Conflict of interest The authors declare that the work involves no conflict of interests. Vicia faba L. (Leguminosae) Ethical approval This article does not contain any studies with human participants or performed by any of the authors. Aphis craccivora: *BRACONIDAE (Hymenoptera): L. gracilis (1). In conlusion, results of the present study reveal natural enemy-aphid-host plant associations and disclose biodiversity of the natural enemies of References aphids in the South Marmara region of northwest Turkey, which is known for having a richly diver- Alford, D. V. (2011). Plant pests. London: Harper Collins sified fauna and flora. Fifty-eight natural enemies, Publishers. 43 aphid species and 58 host plants were identified Amorós-Jiménez, R., Pineda, A., Fereres, A., & Marcos-García, M. A. (2012). Prey availability and abiotic requirements of in the study, and 173 tritrophic associations of them immature stages of the aphid predator Sphaerophoria were determined in all habitats. The vast majority rueppellii. Biological Control, 63,17–24. of identified aphids and species of their natural Aslan, M. M., & Uygun, N. (2005). The aphidophagus coccinellid enemies are new records for the fauna of the South (Coleoptera: Coccinellidae) species in Kahramanmaraş, – Marmara region. We feel that determining biodiver- Turkey. Turkish Journal of Zoology, 29,1 8. – Aslan, M. M., Uygun, N., & Starý, P. (2004). A survey of aphid sity of the natural enemies of aphids including parasitoids in Kahramanmaras, Turkey (Hymenoptera: harmful species that cause economically significant Braconidae: Aphidiinae; and Hymenoptera: ). losses of crops–contributes both to more effective Phytoparasitica, 32(3), 255–263. planning of strategies for biological control of these Bai, B., & Mackauer, M. (1990). Oviposition and host-feeding pests and to creation of an inventory of the region’s patterns in (Hymenoptera: Aphelinidae) at different aphid densities. Ecological Entomology, 15,9–16. faunal biodiversity. It is generally known that a Bankowska, R., Kierych, E., Mikolajczyk, W., Palmowska, J., & high biodiversity of natural enemies strengthens Trojan, P. (1975). Aphid-aphidophage community in alfalfa the possibilities of achieving biological control. cultures (Medicago sativa L.) in Poland. Part I. Structure and However, it should not be forgotten that the rich- phenology of the community. Annales Zoologici, 32(14), 299–345. ness or absence of natural enemy biodiversity can Bayrak, N., & Hayat, R. (2008). Faunistic studies on the species of have either a positive or a negative impact on the Syrphidae (Diptera) in Kayseri province. Bitki Koruma biological control of pests (Jonsson et al. 2017). Bülteni, 48(4), 35–49. Accordingly, it is believed that research in the Blackman, R. L., & Eastop, V. F. (2006). Aphids on the world's future should be focused on the mechanisms herbaceous plants and shrubs. Natural History Museum, London: John Wiley & Sons Ltd.. governing interactions between natural enemies, Blackman R. L., & Eastop, V. F. (2018). Aphids on the world's pests and their host plants in to increase the plants: an online ıdentification and ınformation guide. chances for success of biological pest control. http://www.aphidsonworldsplants.info Phytoparasitica

Çerçi, B., & Koçak, Ö. (2016). Contribution to knowledge of the Letourneau, D. K., Jedlicka, J. A., Bothwell, S. G., & Moreno, S. Heteroptera (Hemiptera) fauna of Turkey. Journal of R. (2009). Effects of natural enemy biodiversity on the sup- Biodiversity, 4(15), 1–18. pression of arthropod herbivores in terrestrial ecosystems. Çetin Erdoğan, Ö., Tomanović, Ž., & Beyarslan, A. (2008). New Annual Review of Ecology, , and Systematics, 40, aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in 573–592. the region of Marmara. Acta Entomologica Serbica, 13,85– Lu, Y. H., Wu, K. M., Jiang, Y. Y., Guo, Y. Y., & Desneux, N. 88. (2012). Widespread adoption of Bt cotton and insecticide Chambers, R. J. (1988). Syrphidae. In A. K. Minks & P. Harrewijn decrease promotes biocontrol services. Nature, 487,362– (Eds.), Aphids, their biology, natural enemies and control 365. (pp. 259–270). Amsterdam: Elsevier. Malinowska, D. (1973). Larvae of hoverflies (Diptera: Syrphidae) Cisneros, J. J., & Rosenheim, J. A. (1997). Ontogenetic change of in aphid colonies on some cultivated plants. Polskie Pismo prey preference in the generalist predator Zelus renardii and Entomologiczne, 43,607–619. its influence on predator-predator interactions. Ecological Marcos García, M. A. (1981). Contribución al conocimento de los Entomology, 22,399–407. Syrphidae (Diptera) de la zona noroeste de la provincia de Cronin, J. P., Welsh, M. E., Dekkers, M. G., Abercrombie, S. T., & Salamanca. Bolletín de la Asociación española de Mitchel, C. E. (2010). Host physiological phenotype explains Entomología, 4,157–171. pathogen reservoir potential. Ecology Letters, 13, 1221– Marcos García, M. A. (1985). Sirphidofauna de las sierras de 1232. Béjar, La Alberca y Gata. Subfamilia Syrphinae (Syrpinae, Davranoglou, L. R. (2011). Zelus renardii (Kolenati, 1856), a new Diptera). Revista Provincial de Estudios, 16(17), 389–419. world reduviid discovered in Europe (Hemiptera: Mattson, W. J. (1980). Herbivory in relation to plant nitrogen : ). Entomologist’s Monthly content. Annual Review of Ecology and Systematics, 11, Magazine, 147(1766–1768), 157–162. 119–161. Diehl, E., Sereda, E., Wolters, V., & Birkhofer, K. (2013). Effects Michaud, J. P., & Mackauer, M. (1994). The use of visual cues in of predator specialization, host plant and climate on biolog- host evaluation by aphidiid . 1. Comparison between 3 ical control of aphids by natural enemies: A meta-analysis. Aphidius parasitoids of the pea aphid. Entomologia Journal of Applied Ecology, 50,262–270. Experimentalis et Applicata, 70,273–283. Gomes, A. (1981). Sirfíeos colhidos em Portugal durante 1977 Montoya, J. M., Rodriguez, M. A., & Hawkins, B. A. (2003). (Diptera: Syrphidae). Agronomia Lusitana, 41(1), 5–24. Food web complexity and higher-level ecosystem services. Griffin, J. N., Byrnes, J. E. K., & Cardinale, B. J. (2013). Effects of Ecology Letters, 6,587–593. predator richness on prey suppression: A meta-analysis. Nakashima, Y., & Akashi, M. (2005). Temporal and within-plant Ecology, 94,2180–2187. distribution of the parasitoid and predator complexes associ- Harmon, J. P., Losey, J. E., & Ives, A. R. (1998). The role of vision ated with Acyrthosiphon pisum and A. kondoi (Homoptera: and colour in the close proximity foraging behaviour of four Aphididae) on alfalfa in Japan. Japanese Applied coccinellid species. Oecologia, 115,287–292. Entomology and Zoology, 40(1), 137–144. Hatano, E., Kunert, G., Michaud, J. P., & Weisser, W. W. (2008). Ölmez, S., & Ulusoy, M. R. (2003). A survey of aphid parasitoids Chemical cues mediating aphid location by natural enemies. (Hymenoptera: Braconidae: Aphidiinae) in Diyarbakır, European Journal of Entomology, 105,797–806. Turkey. Phytoparasitica, 31(5), 524–528. Jonsson, M., Kaartinen, R., & Straub, C. S. (2017). Relationships Özhatay, N., & Özhatay, E. (2005). Kazdağı.InN.Özhatay,A. between natural enemy diversity and biological control. Byfield, & S. Atay (Eds.), Turkiye’nin 122 Onemli Bitki Alanı Current Opinion in Insect Science, 20,1–6. (pp. 73–76). İstanbul: Turkiye Doğal Hayatı Koruma Vakfı. Katano, I., Doi, H., Eriksson, B. K., & Hillebrand, H. (2015). A Pineda, A., & García, M. (2008). Seasonal abundance of cross-system meta analysis reveals coupled effects aphidophagous hoverflies (Diptera: Syrphidae) and their on prey biomass and diversity. Oikos, 124,1427–1435. population levels in and outside Mediterranean sweet pepper Kök, Ş., & Kasap, İ. (2019). Aphid (Hemiptera: Aphididae) spe- greenhouses. Annals of the Entomological Society of cies of the South Marmara region of Turkey including the America, 101(2), 384–391. first record of Dysaphis radicola meridialis Shaposhnikov, Rakhshani, E., Talebi, A. A., Manzari, S., Rezwani, A., & 1964 for the aphid fauna of Turkey. Turkish Journal of Rakhshani, H. (2006). An investigation on alfalfa aphids Entomology, 43(1), 63–78. and their parasitoids in different parts of Iran, with a key to Kök, Ş., Kasap, İ., & Özdemir, I. (2016). Aphid (Hemiptera: the parasitoids (Hemiptera: Aphididae; Hymenoptera: Aphididae) species determined in Çanakkale Province with Braconidae: Aphidiinae). Journal of the Entomological a new record for the aphid fauna of Turkey. Turkish Journal Society of Iran, 25(2), 1–14. of Entomology, 40(4), 397–412. Ralec, A. L. (1995). Egg contents in relation to host-feeding in Kök, Ş., Tomanović, Ž., Şenal, D., Baştuğ, G., & Kasap, İ. (2017). some parasitic Hymenoptera. Entomophaga, 40,87–93. Aphidophagous coccinellid and parasitoid species deter- Read, D. P., Feeny, P.P., & Root, R. B. (1970). Habitat selection by mined in the Çanakkale Province with a new record for the the aphid parasite Diaretiella rapae (Hymenoptera: parasitoid fauna of Turkey. Bitki Koruma Bülteni, 57(4), Braconidae) and hyperparasite Charips brassicae 485–502. (Hymenoptera: Cynipidae). Canadian Entomologist, 102, Leroy, P. D., Verheggen, F. J., Capella, Q., Francis, F., & 1567–1578. Haubruge, E. (2010). An introduction device for the Rojo, S., & Marcos García, M. A. (1998). Catálogo de los sírfidos aphidophagous hoverfly Episyrphus balteatus (De Geer) (Diptera: Syrphidae) afidófagos (Homoptera: Aphididae) (Diptera: Syrphidae). Biological Control, 54,181–188. presentes en los cultivos y plantas herbáceas de España y Phytoparasitica

Portugal. Bolletino di Zoologia agraria e di Bachicoltura, Braconidae, Aphidiinae) from Turkey. Periodicum Ser. II, 30(1), 39–54. Biologorum, 110(4), 335–338. Rojo, S., Gilbert, F. S., Marcos García, M. A., Nieto, J. M., & van Lenteren, J. C., Bale, J., Bigler, F., Hokkanen, H. M. T., & Mier,M.P.(2003).A world review of predatory hoverflies Loomans, A. J. M. (2006). Assessing risks of releasing exotic (Diptera: Syrphidae: Syrphinae) and their prey (319 pp). biological control agents of arthropod pests. Annual Review Alicante: Centro Iberoamericano de la Biodiversidad of Entomology, 51,609–634. (CIBIO). Völkl, W., Mackauer, M., Pell, J. K., & Brodeur, J. (2007). Rosenheim, J. A., Wilhoit, L. R., & Armer, C. A. (1993). Influence Predators, parasitoids and pathogens. In H. F. van Emden & of among generalist insect predators on R. Harrington (Eds.), Aphids as crop pests (pp. 187–233). the suppression of an herbivore population. Oecologia, 96, Oxford: Oxford University Press. – 439 449. Waage, J. K. (1991). Biodiversity as a resource for biological Sadeghi, H., & Gilbert, F. (2000). Aphid suitability and its rela- control. In D. L. Hawksworth (Ed.), The biodiversity of tionship to oviposition preference in predatory hoverflies. microorganisms and invertebrates: Its role in sustainable – Journal of Ecology, 69(5), 771 784. agriculture (pp. 149–163). Wallingford: CAB International. Schütz, K., Bonkowski, M., & Scheu, S. (2008). Effects of Walton,P.D.(1983).Production and management of cultivated Collembola and fertilizers on plant performance (Triticum forages. Reston: Reston Publishing Company, Inc.. aestivum) and aphid reproduction (Rhopalosiphum padi). Weirauch, C., Alvarez, C., & Zhang, G. (2012). Zelus renardii and Basic and Applied Ecology, 9,182–188. Z. tetracanthus (Hemiptera: Reduviidae): Biological attri- Simov, N., Gradinarov, D., & Davranoglou, L. R. (2017). Three butes and the potential for dispersal in two assassin bug new assassin bug records (Hemiptera: Heteroptera: species. Florida Entomologist, 95(3), 641–649. Reduviidae) for the Balkan Peninsula. Ecologica – Yurt, N. T., & Karaca, İ. (2018). İzmir ilinde Glycaspis Montenegrina, 13,25 29. ‘ Snyder, W. E., & Wise, D. H. (2001). Contrasting brimblecombei (Moore) (Hemiptera: Aphalaridae) nin Eucalyptus camaldulensis Dehnh üzerinde popülasyon generated by a community of generalist predators. Ecology, ğ ş ı 82, 1571–1583. de i imi ve bu alanda bulunan yararl türler. Süleyman Demirel Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 22, Summers, C. G. (1976). Population fluctuations of selected arthro- – pods in alfalfa: Influence of two harvest practices. 83 88. Environmental Entomology, 5(1), 103–110. Zhu, J. W., & Park, K. C. (2005). Methyl salicylate, a soybean Summers, C. G. (1998). Integrated pest management in forage aphid-induced plant volatile attractive to the predator alfalfa. Integrated Pest Management Reviews, 3,127–154. Coccinella septempunctata. Journal of Chemical Ecology, – Symondson, W. O. C., Sunderland, K. D., & Greenstone, M. H. 31, 1733 1746. (2002). Can generalist predators be effective biocontrol agents? Annual Review of Entomology, 47,561–594. Publisher’snoteSpringer Nature remains neutral with regard to Tomanović, Ž., Beyarslan, A., Çetin Erdoğan, Ö., & Žikić,V. jurisdictional claims in published maps and institutional affiliations. (2008). New records of aphid parasitoids (Hymenoptera,